The nutritional phenome of EMT-induced cancer stem-like cells

Oncotarget

Volumn 5, Issue 12, 2014, Pages 3970-3982

  Cuyàs, Elisabet ^a,b   Corominas Faja, Bruna ^a,b   Menendez, Javier A ^a,b  

^a CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^b GIRONA BIOMEDICAL RESEARCH INSTITUTE IDIBGI   (Spain)

Author keywords

Cancer; Cancer stem cells; EMT; Metabolism; Nutrients; Phenome

Indexed keywords

LACTIC ACID; PYRUVIC ACID;

ARTICLE; BREAST CANCER; CANCER STEM CELL; CARBON UTILIZATION; CELL ACTIVATION; CELL EXPANSION; CELL POPULATION; ENERGY YIELD; EPITHELIAL MESENCHYMAL TRANSITION; FUNCTIONAL GENOMICS; GENETIC ASSOCIATION; GLYCOLYSIS; HUMAN; MITOCHONDRIAL RESPIRATION; NITROGEN UTILIZATION; NONHUMAN; NUTRIENT; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; FEMALE; FOOD; METABOLISM; PATHOLOGY; TUMOR CELL LINE; UTILIZATION;

CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FOOD; HUMANS; NEOPLASTIC STEM CELLS; PHENOTYPE;

EID: 84905105766     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2147     Document Type: Article

References (89)

1. WARBURG O. On the origin of cancer cells. Science. 1956; 123:309-314.
2. Warburg, O. On respiratory impairment in cancer cells. Science. 1956; 124: 269-270.
3. Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011; 11:325-337.
4. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell. 2008;13:472-482.
5. Jones RG, Thompson CB. Tumor suppressors and cell metabolism: a recipe for cancer growth. Genes Dev. 2009; 23:537-548.
6. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
7. Menendez JA, Joven J, Cufí S, Corominas-Faja B, Oliveras-Ferraros C, Cuyàs E, Martin-Castillo B, López-Bonet E, Alarcón T, Vazquez-Martin A. The Warburg effect version 2.0: metabolic reprogramming of cancer stem cells. Cell Cycle. 2013; 12:1166-1179.
8. Guan JL, Simon AK, Prescott M, Menendez JA, Liu F, Wang F, Wang C, Wolvetang E, Vazquez-Martin A, Zhang J. Autophagy in stem cells. Autophagy. 2013;9:830-849.
9. Vlashi E, Lagadec C, Vergnes L, Matsutani T, Masui K, Poulou M, Popescu R, Della Donna L, Evers P, Dekmezian C, Reue K, Christofk H, Mischel PS, Pajonk F. Metabolic state of glioma stem cells and nontumorigenic cells. Proc Natl Acad Sci U S A. 2011; 108:16062-16067.
10. Goidts V, Bageritz J, Puccio L, Nakata S, Zapatka M, Barbus S, Toedt G, Campos B, Korshunov A, Momma S, Van Schaftingen E, Reifenberger G, Herold-Mende C, Lichter P, Radlwimmer B. RNAi screening in glioma stem-like cells identifies PFKFB4 as a key molecule important for cancer cell survival. Oncogene. 2012; 31:3235-3243.
11. Feng W, Gentles A, Nair RV, Huang M, Lin Y, Lee CY, Cai S, Scheeren FA, Kuo AH, Diehn M. Targeting Unique Metabolic Properties of Breast Tumor Initiating Cells. Stem Cells. 2014 Feb 4. doi: 10.1002/stem.1662.
12. Palorini R, Votta G, Balestrieri C, Monestiroli A, Olivieri S, Vento R, Chiaradonna F. Energy metabolism characterization of a novel cancer stem cell-like line 3AB-OS. J Cell Biochem. 2014; 115:368-379.
13. Mihaylova MM, Sabatini DM, Yilmaz ÖH. Dietary and metabolic control of stem cell function in physiology and cancer. Cell Stem Cell. 2014;14:292-305.
14. Menendez JA, Alarcón T, Corominas-Faja B, Cuyàs E, López-Bonet E, Martin AG, Vellon L. Xenopatients 2.0: reprogramming the epigenetic landscapes of patient-derived cancer genomes. Cell Cycle. 2014;13:358-370.
15. Zhang J, Nuebel E, Daley GQ, Koehler CM, Teitell MA. Metabolic regulation in pluripotent stem cells during reprogramming and self-renewal. Cell Stem Cell. 2012;11:589-595.
16. Rafalski VA, Mancini E, Brunet A. Energy metabolism and energy-sensing pathways in mammalian embryonic and adult stem cell fate. J Cell Sci. 2012; 125:5597-5608.
17. Riggs JW, Barrilleaux BL, Varlakhanova N, Bush KM, Chan V, Knoepfler PS. Induced pluripotency and oncogenic transformation are related processes. Stem Cells Dev. 2013;22:37-50.
18. Shyh-Chang N, Daley GQ, Cantley LC. Stem cell metabolism in tissue development and aging. Development. 2013; 140:2535-2547.
19. Ochocki JD, Simon MC. Nutrient-sensing pathways and metabolic regulation in stem cells. J Cell Biol. 2013; 203:23-33.
20. Ito K, Suda T. Metabolic requirements for the maintenance of self-renewing stem cells. Nat Rev Mol Cell Biol. 2014;15:243-256.
21. Dong C, Yuan T, Wu Y, Wang Y, Fan TW, Miriyala S, Lin Y, Yao J, Shi J, Kang T, Lorkiewicz P, St Clair D, Hung MC, Evers BM, Zhou BP. Loss of FBP1 by Snail-mediated repression provides metabolic advantages in basal-like breast cancer. Cancer Cell. 2013;23:316-331.
22. Liu PP, Liao J, Tang ZJ, Wu WJ, Yang J, Zeng ZL, Hu Y, Wang P, Ju HQ, Xu RH, Huang P. Metabolic regulation of cancer cell side population by glucose through activation of the Akt pathway. Cell Death Differ. 2014;21:124-135.
23. Del Barco S, Vazquez-Martin A, Cufí S, Oliveras-Ferraros C, Bosch-Barrera J, Joven J, Martin-Castillo B, Menendez JA. Metformin: multi-faceted protection against cancer. Oncotarget. 2011; 2:896-917.
24. Vazquez-Martin A, López-Bonetc E, Cufí S, Oliveras-Ferraros C, Del Barco S, Martin-Castillo B, Menendez JA. Repositioning chloroquine and metformin to eliminate cancer stem cell traits in pre-malignant lesions. Drug Resist Updat. 2011; 14:212-223.
25. Vazquez-Martin A, CufiS, Lopez-Bonet E, Corominas-Faja B, Oliveras-Ferraros C, Martin-Castillo B, Menendez JA. Metformin limits the tumourigenicity of iPS cells without affecting their pluripotency. Sci Rep. 2012;2:964.
26. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008; 133:704-715.
27. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009; 138:645-659.
28. Bochner BR, Gadzinski P, Panomitros E. Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res. 2001; 11:1246-1255.
29. Bochner BR. Global phenotypic characterization of bacteria. FEMS Microbiol Rev. 2009; 33:191-205.
30. Bochner BR, Siri M, Huang RH, Noble S, Lei XH, Clemons PA, Wagner BK. Assay of the multiple energy-producing pathways of mammalian cells. PLoS One. 2011; 6:e18147.
31. Shea A, Wolcott M, Daefler S, Rozak DA. Biolog phenotype microarrays. Methods Mol Biol. 2012; 881:331-373.
32. Mackie AM, Hassan KA, Paulsen IT, Tetu SG. Biolog Phenotype Microarrays for phenotypic characterization of microbial cells. Methods Mol Biol. 2014; 1096:123-130.
33. Houle D, Govindaraju DR, Omholt S. Phenomics: the next challenge. Nat Rev Genet. 2010;11:855-866.
34. Lanktree MB, Hassell RG, Lahiry P, Hegele RA. Phenomics: expanding the role of clinical evaluation in genomic studies. J Investig Med. 2010; 58:700-706.
35. Zbuk KM, Eng C. Cancer phenomics: RET and PTEN as illustrative models. Nat Rev Cancer. 2007;7:35-45.
36. Chaffer CL, Marjanovic ND, Lee T, Bell G, Kleer CG, Reinhardt F, D'Alessio AC, Young RA, Weinberg RA. Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity. Cell. 2013; 154:61-74.
37. Marjanovic ND, Weinberg RA, Chaffer CL. Poised with purpose: cell plasticity enhances tumorigenicity. Cell Cycle. 2013;12:2713-2714.
38. Ansieau S. EMT in breast cancer stem cell generation. Cancer Lett. 2013; 338:63-68.
39. Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature. 2013; 501:328-337.
40. Marjanovic ND, Weinberg RA, Chaffer CL. Cell plasticity and heterogeneity in cancer. Clin Chem. 2013; 59:168-179.
41. Iliopoulos D, Hirsch HA, Struhl K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell. 2009; 139:693-706.
42. Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, Lander ES. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell. 2011; 146:633-644.
43. Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO, Brooks M, Reinhardt F, Su Y, Polyak K, Arendt LM, Kuperwasser C, Bierie B, Weinberg RA. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci U S A. 2011; 108:7950-7955.
44. Iliopoulos D, Hirsch HA, Wang G, Struhl K. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci U S A. 2011; 108:1397-1402.
45. Polytarchou C, Iliopoulos D, Struhl K. An integrated transcriptional regulatory circuit that reinforces the breast cancer stem cell state. Proc Natl Acad Sci U S A. 2012; 109:14470-14475.
46. Sonveaux P, Végran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, De Saedeleer CJ, Kennedy KM, Diepart C, Jordan BF, Kelley MJ, Gallez B, Wahl ML, Feron O, Dewhirst MW. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest. 2008; 118:3930-3942.
47. Semenza GL. Tumor metabolism: cancer cells give and take lactate. J Clin Invest. 2008; 118:3835-3837.
48. Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, Pestell RG, Martinez-Outschoorn UE, Sotgia F, Lisanti MP. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle. 2009; 8:3984-4001.
49. Pavlides S, Tsirigos A, Vera I, Flomenberg N, Frank PG, Casimiro MC, Wang C, Pestell RG, Martinez-Outschoorn UE, Howell A, Sotgia F, Lisanti MP. Transcriptional evidence for the "Reverse Warburg Effect" in human breast cancer tumor stroma and metastasis: similarities with oxidative stress, inflammation, Alzheimer's disease, and "Neuron-Glia Metabolic Coupling". Aging (Albany NY). 2010; 2:185-199.
50. Bonuccelli G, Whitaker-Menezes D, Castello-Cros R, Pavlides S, Pestell RG, Fatatis A, Witkiewicz AK, Vander Heiden MG, Migneco G, Chiavarina B, Frank PG, Capozza F, Flomenberg N, Martinez-Outschoorn UE, Sotgia F, Lisanti MP. The reverse Warburg effect: glycolysis inhibitors prevent the tumor promoting effects of caveolin-1 deficient cancer associated fibroblasts. Cell Cycle. 2010; 9:1960-1971.
51. Migneco G, Whitaker-Menezes D, Chiavarina B, Castello-Cros R, Pavlides S, Pestell RG, Fatatis A, Flomenberg N, Tsirigos A, Howell A, Martinez-Outschoorn UE, Sotgia F, Lisanti MP. Glycolytic cancer associated fibroblasts promote breast cancer tumor growth, without a measurable increase in angiogenesis: evidence for stromal-epithelial metabolic coupling. Cell Cycle. 2010; 9:2412-2422.
52. Martinez-Outschoorn UE, Balliet RM, Rivadeneira DB, Chiavarina B, Pavlides S, Wang C, Whitaker-Menezes D, Daumer KM, Lin Z, Witkiewicz AK, Flomenberg N, Howell A, Pestell RG, Knudsen ES, Sotgia F, Lisanti MP. Oxidative stress in cancer associated fibroblasts drives tumor-stroma co-evolution: A new paradigm for understanding tumor metabolism, the field effect and genomic instability in cancer cells. Cell Cycle. 2010; 9:3256-3276.
53. Bonuccelli G, Tsirigos A, Whitaker-Menezes D, Pavlides S, Pestell RG, Chiavarina B, Frank PG, Flomenberg N, Howell A, Martinez-Outschoorn UE, Sotgia F, Lisanti MP. Ketones and lactate "fuel" tumor growth and metastasis: Evidence that epithelial cancer cells use oxidative mitochondrial metabolism. Cell Cycle. 2010; 9:3506-3514.
54. Whitaker-Menezes D, Martinez-Outschoorn UE, Lin Z, Ertel A, Flomenberg N, Witkiewicz AK, Birbe RC, Howell A, Pavlides S, Gandara R, Pestell RG, Sotgia F, Philp NJ, Lisanti MP. Evidence for a stromal-epithelial "lactate shuttle" in human tumors: MCT4 is a marker of oxidative stress in cancer-associated fibroblasts. Cell Cycle. 2011; 10:1772-1783.
55. Fiaschi T, Marini A, Giannoni E, Taddei ML, Gandellini P, De Donatis A, Lanciotti M, Serni S, Cirri P, Chiarugi P. Reciprocal metabolic reprogramming through lactate shuttle coordinately influences tumor-stroma interplay. Cancer Res. 2012;72:5130-5140.
56. Salem AF, Whitaker-Menezes D, Lin Z, Martinez-Outschoorn UE, Tanowitz HB, Al-Zoubi MS, Howell A, Pestell RG, Sotgia F, Lisanti MP. Two-compartment tumor metabolism: autophagy in the tumor microenvironment and oxidative mitochondrial metabolism (OXPHOS) in cancer cells. Cell Cycle. 2012; 11:2545-2556.
57. Guido C, Whitaker-Menezes D, Capparelli C, Balliet R, Lin Z, Pestell RG, Howell A, Aquila S, Andò S, Martinez-Outschoorn U, Sotgia F, Lisanti MP. Metabolic reprogramming of cancer-associated fibroblasts by TGF-β drives tumor growth: connecting TGF-β signaling with "Warburg-like" cancer metabolism and L-lactate production. Cell Cycle. 2012; 11:3019-3035.
58. Martinez-Outschoorn UE, Lin Z, Whitaker-Menezes D, Howell A, Lisanti MP, Sotgia F. Ketone bodies and two-compartment tumor metabolism: stromal ketone production fuels mitochondrial biogenesis in epithelial cancer cells. Cell Cycle. 2012;11:3956-3963.
59. Martinez-Outschoorn UE, Lin Z, Whitaker-Menezes D, Howell A, Sotgia F, Lisanti MP. Ketone body utilization drives tumor growth and metastasis. Cell Cycle. 2012; 11:3964-3971.
60. Capparelli C, Guido C, Whitaker-Menezes D, Bonuccelli G, Balliet R, Pestell TG, Goldberg AF, Pestell RG, Howell A, Sneddon S, Birbe R, Tsirigos A, Martinez-Outschoorn U, Sotgia F, Lisanti MP. Autophagy and senescence in cancer-associated fibroblasts metabolically supports tumor growth and metastasis via glycolysis and ketone production. Cell Cycle. 2012; 11:2285-2302.
61. Lisanti MP, Martinez-Outschoorn UE, Sotgia F. Oncogenes induce the cancer-associated fibroblast phenotype: metabolic symbiosis and "fibroblast addiction" are new therapeutic targets for drug discovery. Cell Cycle. 2013; 12:2723-2732.
62. Sanchez-Alvarez R, Martinez-Outschoorn UE, Lamb R, Hulit J, Howell A, Gandara R, Sartini M, Rubin E, Lisanti MP, Sotgia F. Mitochondrial dysfunction in breast cancer cells prevents tumor growth: understanding chemoprevention with metformin. Cell Cycle. 2013; 12:172-182.
63. Sotgia F, Martinez-Outschoorn UE, Lisanti MP. Cancer metabolism: new validated targets for drug discovery. Oncotarget. 2013; 4:1309-1316.
64. Martinez-Outschoorn U, Sotgia F, Lisanti MP. Tumor microenvironment and metabolic synergy in breast cancers: critical importance of mitochondrial fuels and function. Semin Oncol. 2014;41:195-216.
65. Martinez-Outschoorn UE, Lisanti MP, Sotgia F. Catabolic cancer-associated fibroblasts transfer energy and biomass to anabolic cancer cells, fueling tumor growth. Semin Cancer Biol. 2014; 25:47-60.
66. Zhou W, Mukherjee P, Kiebish MA, Markis WT, Mantis JG, Seyfried TN. The calorically restricted ketogenic diet, an effective alternative therapy for malignant brain cancer. Nutr Metab (Lond). 2007; 4:5.
67. Stafford P, Abdelwahab MG, Kim do Y, Preul MC, Rho JM, Scheck AC. The ketogenic diet reverses gene expression patterns and reduces reactive oxygen species levels when used as an adjuvant therapy for glioma. Nutr Metab (Lond). 2010;7:74.
68. Maurer GD, Brucker DP, Bähr O, Harter PN, Hattingen E, Walenta S, Mueller-Klieser W, Steinbach JP, Rieger J. Differential utilization of ketone bodies by neurons and glioma cell lines: a rationale for ketogenic diet as experimental glioma therapy. BMC Cancer. 2011;11:315.
69. Abdelwahab MG, Fenton KE, Preul MC, Rho JM, Lynch A, Stafford P, Scheck AC. The ketogenic diet is an effective adjuvant to radiation therapy for the treatment of malignant glioma. PLoS One. 2012; 7:e36197.
70. Champ CE, Palmer JD, Volek JS, Werner-Wasik M, Andrews DW, Evans JJ, Glass J, Kim L, Shi W. Targeting metabolism with a ketogenic diet during the treatment of glioblastoma multiforme. J Neurooncol. 2014;117:125-131.
71. Kennedy KM, Scarbrough PM, Ribeiro A, Richardson R, Yuan H, Sonveaux P, Landon CD, Chi JT, Pizzo S, Schroeder T, Dewhirst MW. Catabolism of exogenous lactate reveals it as a legitimate metabolic substrate in breast cancer. PLoS One. 2013; 8:e75154.
72. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell. 2005; 8:299-309.
73. Shen R, Ye Y, Chen L, Yan Q, Barsky SH, Gao JX. Precancerous stem cells can serve as tumor vasculogenic progenitors. PLoS One. 2008; 3:e1652.
74. Cabarcas SM, Mathews LA, Farrar WL. The cancer stem cell niche--there goes the neighborhood? Int J Cancer. 2011; 129:2315-2327.
75. Cascone T, Herynk MH, Xu L, Du Z, Kadara H, Nilsson MB, Oborn CJ, Park YY, Erez B, Jacoby JJ, Lee JS, Lin HY, Ciardiello F, Herbst RS, Langley RR, Heymach JV. Upregulated stromal EGFR and vascular remodeling in mouse xenograft models of angiogenesis inhibitor-resistant human lung adenocarcinoma. J Clin Invest. 2011; 121:1313-28.
76. Osawa T, Shibuya M. Targeting cancer cells resistant to hypoxia and nutrient starvation to improve anti-angiogeneic therapy. Cell Cycle. 2013; 12:2519-2520.
77. Philip B, Ito K, Moreno-Sánchez R, Ralph SJ. HIF expression and the role of hypoxic microenvironments within primary tumours as protective sites driving cancer stem cell renewal and metastatic progression. Carcinogenesis. 2013; 34:1699-1707.
78. Mathonnet M, Perraud A, Christou N, Akil H, Melin C, Battu S, Jauberteau MO, Denizot Y. Hallmarks in colorectal cancer: Angiogenesis and cancer stem-like cells. World J Gastroenterol. 2014; 20:4189-4196.
79. Ming Valerie Lin, Gene Bishop, Maria Benito-Herrero. Diabetic Ketoacidosis in Type 2 Diabetics: A Novel Presentation of Pancreatic Adenocarcinoma. J Gen Intern Med. 2010; 25: 369-373.
80. Martinez-Outschoorn UE, Whitaker-Menezes D, Valsecchi M, Martinez-Cantarin MP, Dulau-Florea A, Gong J, Howell A, Flomenberg N, Pestell RG, Wagner J, Arana-Yi C, Sharma M, Sotgia F, Lisanti MP. Reverse Warburg effect in a patient with aggressive B-cell lymphoma: is lactic acidosis a paraneoplastic syndrome? Semin Oncol. 2013; 40:403-418.
81. Bijland LR, Bomers MK, Smulders YM. Smelling the diagnosis: a review on the use of scent in diagnosing disease. Neth J Med. 2013; 71:300-307.
82. Riscuta G, Dumitrescu RG. Nutrigenomics: implications for breast and colon cancer prevention. Methods Mol Biol. 2012; 863:343-358.
83. Ferguson LR, Schlothauer RC. The potential role of nutritional genomics tools in validating high health foods for cancer control: broccoli as example. Mol Nutr Food Res. 2012;56:126-146.
84. Lundstrom K. Past, present and future of nutrigenomics and its influence on drug development. Curr Drug Discov Technol. 2013; 10:35-46.
85. Levesque JP, Winkler IG, Rasko JE. Nichotherapy for stem cells: there goes the neighborhood. Bioessays. 2013; 35:183-290.
86. Steinhauser ML, Bailey AP, Senyo SE, Guillermier C, Perlstein TS, Gould AP, Lee RT, Lechene CP. Multi-isotope imaging mass spectrometry quantifies stem cell division and metabolism. Nature. 2012; 481:516-519.
87. Steinhauser ML, Lechene CP. Quantitative imaging of subcellular metabolism with stable isotopes and multi-isotope imaging mass spectrometry. Semin Cell Dev Biol. 2013; 24:661-667.
88. Blagosklonny MV. Cancer stem cell and cancer stemloids: from biology to therapy. Cancer Biol Ther. 2007; 6:1684-1690.
89. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003; 100:3983-3988.